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Field dodder (Cuscuta campestris) does not promote nutrient transfer between parasitized host plants.

Recent phylogenetic analyses rank parasitism as the most common consumer strategy among heterotrophic organisms (De Meeu and Renaud, 2002). Numerous ecological studies indicate that parasites can have profound ecosystem-level effects by influencing competitive interactions (Feener, 1981; Combes, 1996), community composition (Combes, 1996; Mouritsen and Poulin, 2010), and trophic energy flow (Lafferty et al., 2008), but the majority of these studies have focused exclusively on animal parasites. In comparison, the ecology of well-known parasitic plants, many of which are economically destructive agricultural pests, remains understudied (but see Callaway and Pennings, 1998; Marvier, 1998; Mueller and Gehring, 2006).

Like animal parasites, parasitic plants can have substantial effects on individual host growth and reproduction (Press and Graves, 1995) as well as ecosystem structure and productivity (Press and Phoenix, 2005; Bardgett et al., 2006). For instance, dwarf mistletoe (Arceuthobium spp.) not only increases the likelihood of herbivore-induced tree mortality in ponderosa pine (Pinus ponderosa; Parker et al., 2006) it also considerably alters forest fire dynamics (Hoffman et al., 2007). In addition to landscape-level changes, parasitic plants can have indirect and often cryptic effects on multispecies interactions. In Australia, the native hemiparasitic vine, Cassytha pubescens (Loranthaceae), modifies interactions among three nonnative species: a pollinator (Apis mellifera), a seed predator (Bruchidius villosus), and the invasive legume Cytisus scoparius (Prider et al., 2011). In particular, the reduced reproductive output of parasitized Cytisus plants indirectly impacts species that depend on these resources, including B. villosus and A. mellifera (Prider et al., 2011).

Dodders (Cuscuta spp.) are globally distributed, angiosperm parasitic plants. Due to their limited photosynthetic ability, dodder seedlings are entirely dependent on the host for resources and must become established on a host shortly after germinating (Costea and Tardif, 2006). Using volatile cues, a seedling locates a suitable host (Runyon et al., 2006) and forms tight coils around its stem. In order to penetrate the host vascular tissue, the dodder seedling then produces specialized structures called haustoria, which form direct connections with the phloem and xylem (Birschwilks et al., 2006). This "extraordinarily successful vegetative graft" (Kuijt, 1983:1) allows the dodder parasite to efficiently divert host resources toward its own rapid growth and reproduction.

Because dodder maintains direct associations with host vascular tissue and can parasitize multiple plants simultaneously (Kelly and Homing, 1999), plant pathologists have long utilized it as a vector for viruses (Bennett, 1940). More recently, studies have shown that several macromolecules move from the host plant to dodder, including proteins (Haupt et al., 2001) and phloem-mobile mRNA transcripts (Roney et al., 2007). Smaller molecules, such as sucrose, can move from host to dodder as well as between hosts via dodder (Littlefield et al., 1966; Birschwilks et al., 2006). Given the mounting evidence that materials can move from host to parasite and among multiple parasitized hosts, it is possible that dodder might act as a conduit for other biologically important molecules such as photosynthates and mineral nutrients. In oligotrophic environments, even the movement of relatively small amounts of mineral nutrients among plants could have substantial community-level impacts. For instance, the effects of spatially discrete phenomena (i.e., localized resource pulses) could disperse throughout a community via dodder, influencing competitive interactions and potentially facilitating species coexistence.

Using field dodder (Cuscuta campestris) as a live bridge between plants, this study investigated the movement of nutrients between tomato plants (Solanum lycopersicum) parasitized by dodder. In particular, I sought to address two questions: 1) If two hosts are connected by dodder, does nutrient supplementation for one host plant lead to an increased growth rate in the second (unmanipulated) host plant? 2) Does shading one host plant lead to a reduced growth rate in a connected host plant? Based on past evidence that a variety of molecules, including sucrose, can move between host plants as well as among parasitized hosts via dodder (Littlefield et al., 1966; Haupt et al., 2001; Birschwilks et al., 2006; Roney et al., 2007), I predicted that nutrient supplementation for one host plant would lead to increased growth in a second host plant to which it was connected by field dodder. Similarly, I hypothesized that artificial light limitation for one host plant would reduce its growth rate, leading to an increased rate of nutrient absorption from the second unmanipulated plant by dodder and a reduction in its growth rate.

MATERIALS AND METHODS--I grew tomato seedlings (Solanum lycopersicum, 'Bonnie Best' variety) in University of California Davis Agronomy Soil Mix (40% washed sand, 20% sphagnum peat moss, 20% redwood compost, and 20% pumice rock) in a greenhouse at 20-25[degrees]C with a daily light regime of 16 h light. To establish live bridge host-parasite systems among pairs of plants, I collected 20-cm cuttings of the apical region of C. campestris from a local tomato field in August 2012 (Davis, California) and placed them on the stems of 2-week-old tomato seedlings (Jeschke et al., 1994). To prevent desiccation during the attachment phase, I misted dodder cuttings with distilled water daily. After 7 days, the dodder cuttings began to form haustoria and attach to the seedlings. Within 2-3 days of dodder attachment to the first host (hereafter referred to as the "donor" plant), I allowed the apical region of the dodder plant to attach to the stem of a second tomato plant whose height was within [+ or -]2 cm (the "receiver" plant; Birschwilks et al., 2006). To ensure that the live bridge remained intact, I monitored the growth of dodder haustoria on donor and receiver plants throughout the experiment.

Following dodder attachment to pairs of donor and receiver host plants, I randomly assigned plant pairs to one of four treatments: 1) donor plant shaded, 2) donor plant fertilized, 3) donor plant shaded and fertilized, or 4) control. Each treatment initially included 25 replicate pairs of plants, although host and/ or parasite mortality reduced the number of replicates to 22 pairs in the shading and nutrient addition treatments and 21 pairs in the nutrient + shade and control treatments. In the two nutrient-addition treatments (treatments 2 and 3), I fertilized donor plants with 4 g of Osmocote Smart-Release[R] 19-6-12 plant food (The Scotts Company, Marysville, Ohio) at the beginning of the experiment. I measured height and branch number of both donor and receiver tomato plants weekly for 3 weeks in September 2012. After 4 weeks, I assessed all plants visually for signs of leaf chlorosis (yellowing), an indication of deficiency in essential mineral nutrients (Vesk et al., 1966; Fig. 1). I then harvested all root and shoot material (excluding dodder stems), oven-dried it to constant weight, and weighed it to estimate above- and belowground biomass.

Due to the rapid growth rate of the dodder parasite, it was difficult to control the number of stems connecting donor and receiver plants. Therefore, I counted the number of dodder stems connecting each host pair at the end of the experiment and included it as a covariate in the analysis. Although I could not control the number of dodder stems connecting host plant pairs, I maintained stem directionality (i.e., the dodder parasite stems always originated from the donor host plant). Lastly, I mechanically removed dodder flower buds over the course of the experiment to prevent premature parasite senescence.

All data are publicly available through the ONEShare data repository (permanent link: http://n2t.net/ark:/90135/ q1v122q4; primary identifier: ark:/90135/q1v122q4).

Statistical Analyses--I transformed all response variables prior to analysis to account for the nonnormality and heteroscedasticity of the raw data. Using the Box-Cox transformation technique, I used a power transformation of [lambda] = -0.745 to transform all height data. I [log.sub.10] transformed shoot and root biomass and arcsine transformed branch number. Assumptions of residual normality and equal variance were met following transformation for all response variables. Because mortality did not disproportionately impact one treatment over the others (see Materials and Methods), pairs with one or more dead plants were excluded from the analysis.

I used two-way repeated measures analysis of variance (predictor variables: nutrient addition and shade) and Tukey's pairwise comparison test to determine whether donor plants from the four treatments were significantly different in any of the response variables measured. Using the same predictor variables, I used another two-way repeated measures analysis of variance and Tukey pairwise comparison test to assess differences in the response variables among receiver plants in the four treatments. I used regression analysis to test whether the number of dodder stems connecting plant pairs was significantly correlated to the growth of either plant. Lastly, I used binary logistic regression to determine if treatment was a significant predictor of the likelihood of leaf chlorosis in donor plants. All analyses were performed in SAS 9.3 (SAS Institute, Cary, North Carolina).

RESULTS--Nutrient supplementation had a significant effect on donor plant height (two-way analysis of variance, [F.sub.1,81] = 104.26, P < 0.0001), shoot biomass ([F.sub.1,81] = 83.25, P< 0.0001), and root biomass ([F.sub.1,81] = 27.51, P < 0.0001). Significant interactions also existed between shading and nutrient supplementation for shoot biomass, root biomass, and branch number (P < 0.05 for each). Specifically, at low nutrient conditions, no significant differences existed in shoot biomass, root biomass, or branch number between shaded and unshaded plants (Fig. 2). However, when nutrients were added, plants that were grown in the shade had significantly lower shoot biomass, root biomass, and branch number than plants that were left unshaded. Compared to donor plants in the control treatment, donor plants in the nutrient and nutrient + shade treatments were significantly taller (Tukey's pairwise comparison test, P < 0.05 for both) and had higher shoot biomass (P < 0.05 for both). In addition, donor plants in the nutrient treatment had higher root biomass (Tukey's pairwise comparison test, P < 0.05) than control donor plants. In comparison, no significant treatment effects or pairwise differences existed in any response variables measured for receiver plants (Fig. 2).

Based on the results of the logistic regression, nutrient addition was a significant predictor of the probability of leaf chlorosis in donor plants (P < 0.001). The percentage of chlorotic donor plants was low for both the nutrient treatment (4.5%) and the shade + nutrient treatment (0%). In comparison, 72.7% and 100% of donor plants were chlorotic in the shade and control treatments, respectively. I could not repeat logistic regression analyses for receiver plants because all receiver plants were chlorotic, regardless of treatment.

Correlations between the number of dodder stems connecting donor and receiver plants and any of the response variables measured were low and not significant (P > 0.05 and [R.sup.2] < 0.05 for all).

DISCUSSION--Few parasites are able to parasitize multiple individuals of different species simultaneously. As such, the ecological effects of this unique type of coinfection are largely unknown. Using a dodder live-bridge system, this study sought to investigate whether nutrient supplementation and/or shading for one host plant affects the growth rate of an unmanipulated receiver plant.

As expected, nutrient addition led to significantly increased growth in donor tomato plants. These plants were significantly taller and had higher above- and belowground mass than donor plants in the shade and control treatments (Fig. 2). In comparison, unmanipulated receiver plants showed no significant differences in any of the response variables measured, regardless of treatment. In addition, less than 5% of donor plants in the nutrient addition treatment showed signs of leaf chlorosis compared to all of the receiver plants in the same treatment (Fig. 1). Collectively, these results suggest that few (if any) nutrients passed through dodder from the donor to the receiver host plant.

Previous research on dodder physiology may explain why nutrients were not able to pass from one host plant to another through dodder. To fuel its rapid growth, the parasite acts as a strong sink for photosynthates as well as nitrogenous compounds (Jeschke et al., 1994). A number of specialized cells act to efficiently redirect solutes from the host's vascular tissues, including transfer cells that absorb solutes from the host sieve tubes (Gunning and Pate, 1969) and searching hyphae that connect host plasmodesmata (Birschwilks et al., 2006). Because the dodder parasite cannot sustain itself through photosynthesis, it is possible that these highly adaptive absorption structures are designed to reduce nutrient leakage as much as possible. This may explain why previous studies have documented only a small amount of sucrose transfer between host plants via dodder (Littlefield et al., 1966; Birschwilks et al., 2006) Thus, even if nutrient leakage from parasite to host does occur, the concentration of nutrients might be too low to significantly affect host growth rate.

When light availability was reduced for one host plant, the parasite did not appear to compensate by reducing the growth of the second unmanipulated host plant. In fact, the growth of both the donor and receiver plants in the light limitation treatment was very similar to that of the plants in the control treatment. Previous work has shown that the growth rate and nutrient requirements of Cuscuta spp. depend largely on the vigor of the host (Koch et al., 2004; Costea and Tardif, 2006). Thus, for plants in low-nutrient and/or light-limited conditions, it is likely that the parasite remained small and did not exert a substantial demand for nutrients from the receiver plant. Additional experiments that include dodder biomass as a response variable would be necessary to confirm this hypothesis.

CONCLUSIONS--In summary, the results of this study suggest that dodder-mediated nutrient flow among host plants is occurring at very low amounts or not at all. While this study and other greenhouse experiments offer a powerful way to better understand the physiology and host range of Cuscuta spp., field studies of natural populations must be used to examine how parasitic dodder mediates interactions among native species in a more realistic setting. Experiments such as these may not only elucidate mechanisms of species coexistence within communities, they may also enhance our understanding of how this globally distributed group of parasitic plants affects populations, communities, and entire ecosystems.

I gratefully acknowledge W. T. Lanini for providing dodder seed and greenhouse space for this study, L. H. Yang for valuable feedback on experimental design, N. Willits for statistical consulting, and E. Sandoval for technical support.

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Submitted 13 January 2014.

Acceptance recommended by Associate Editor, James E. Moore, 9 April 2014.

SHAHLA FARZAN

Department of Entomology, University of California, Davis, Davis, CA 95616

Correspondent: sfarzan@ucdavis.edu
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